Tenascin-C is associated with cored amyloid-b plaques in Alzheimer disease and pathology burdened cognitively normal elderly

Journal of Neuropathology and Experimental Neurology

Volumn 75, Issue 9, 2016, Pages 868-876

  Mi, Zhiping ^a,c   Halfter, Willi ^b   Abrahamson, Eric E ^a,c   Klunk, William E ^b   Mathis, Chester A ^a   Mufson, Elliott J ^d   Ikonomovic, Milos D ^a,b,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b Department of Neurobiology ^*  (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d Center for Neurological Restoration   (United States)

Author keywords

Alzheimer disease; Astrocytes; Extracellular matrix; Inflammation; Microglia; Tau; Tenascin; amyloid

Indexed keywords

AMYLOID BETA PROTEIN; BIOLOGICAL MARKER; DYE; TAU PROTEIN; TENASCIN; UNCLASSIFIED DRUG; X 34;

AGED; ALZHEIMER DISEASE; AMYLOID PLAQUE; ARTICLE; ASTROCYTE; BLOOD VESSEL; BLOOD VESSEL WALL; BRAIN TISSUE; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; GRAY MATTER; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; MALE; MICROGLIA; NEURITE; NEUROPIL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; VASCULAR AMYLOIDOSIS; WHITE MATTER; BRAIN CORTEX; CHEMISTRY; COGNITION; LONGITUDINAL STUDY; METABOLISM; PATHOLOGY; PHYSIOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; CEREBRAL CORTEX; COGNITION; FEMALE; HUMANS; LONGITUDINAL STUDIES; MALE; PLAQUE, AMYLOID; TENASCIN;

EID: 84991224440     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1093/jnen/nlw062     Document Type: Article

References (72)

1. Masters CL, Simms G, Weinman NA, et al. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci U S A 1985;82:4245-9
2. Kang J, Lemaire HG, Unterbeck A, et al. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 1987;325:733-6
3. Esler WP, Wolfe MS. A portrait of Alzheimer secretases-new features and familiar faces. Science 2001;293:1449-54
4. Griffin WS, Sheng JG, Roberts GW, et al. Interleukin-1 expression in different plaque types in Alzheimer's disease: significance in plaque evolution. J Neuropathol Exp Neurol 1995;54:276-81
5. Atwood CS, Martins RN, Smith MA, et al. Senile plaque composition and posttranslational modification of amyloid-beta peptide and associated proteins. Peptides 2002:23;1343-50
6. McLaurin J, Yang D, Yip CM, et al. Review: modulating factors in amyloid-beta fibril formation. J Struct Biol 2000;130:259-70
7. Snow AD, Mar H, Nochlin D, et al. The presence of heparan sulfate proteoglycans in the neuritic plaques and congophilic angiopathy in Alzheimer's disease. Am J Pathol 1988;133:456-63
8. DeWitt DA, Silver J, Canning DR, et al. Chondroitin sulfate proteoglycans are associated with the lesions of Alzheimer's disease. Exp Neurol 1993;121:149-52
9. Snow AD, Nochlin D, Sekiguichi R, et al. Identification in immunolocalization of a new class of proteoglycan (keratan sulfate) to the neuritic plaques of Alzheimer's disease. Exp Neurol 1996;138:305-17
10. Snow AD, Mar H, Nochlin D, et al. Peripheral distribution of dermatan sulfate proteoglycans (decorin) in amyloid-containing plaques and their presence in neurofibrillary tangles of Alzheimer's disease. J Histochem Cytochem 1992:40;105-13
11. Doehner J, Madhusudan A, Konietzko U, et al. Co-localization of Reelin and proteolytic AbetaPP fragments in hippocampal plaques in aged wildtype mice. J Alzheimers Dis 2010;19:1339-57
12. Cotman SL, Halfter W, Cole GJ. Agrin binds to beta-amyloid (Abeta), accelerates abeta fibril formation, and is localized to Abeta deposits in Alzheimer's disease brain. Mol Cell Neurosci 2000;15: 183-98
13. van Horssen J, Wilhelmus MM, Heljasvaara R, et al. Collagen XVIII: a novel heparan sulfate proteoglycan associated with vascular amyloid depositions and senile plaques in Alzheimer's disease brains. Brain Pathol 2002:12;456-62
14. Hashimoto T, Wakabayashi T, Watanabe A, et al. CLAC: a novel Alzheimer amyloid plaque component derived from a transmembrane precursor, CLAC-P/collagen type XXV. Embo J 2002;21:1524-34
15. Peress N, Perillo E, Zucker S. Localization of tissue inhibitor of matrix metalloproteinases in Alzheimer's disease and normal brain. J Neuropathol Exp Neurol 1995;54:16-22
16. Mencarelli C, Bode GH, Losen M, et al. Goodpasture antigen-binding protein/ceramide transporter binds to human serum amyloid P-component and is present in brain amyloid plaques. J Biol Chem 2012;287: 14897-911
17. Chiquet-Ehrismann R, Tucker RP. Tenascins and the importance of adhesion modulation. Cold Spring Harb Perspect Biol 2011;3:a004960
18. Jones EV, Bouvier DS. Astrocyte-secreted matricellular proteins in CNS remodelling during development and disease. Neural Plast 2014;2014: 321209:1-12
19. Smith GM, Hale JH. Macrophage/Microglia regulation of astrocytic tenascin: synergistic action of transforming growth factor-beta and basic fibroblast growth factor. J Neurosci 1997;17:9624-33
20. Laywell ED, Dorries U, Bartsch U, et al. Enhanced expression of the developmentally regulated extracellular matrix molecule tenascin following adult brain injury. Proc Natl Acad Sci U S A 1992;89:2634-8
21. Roll L, Faissner A. Influence of the extracellular matrix on endogenous and transplanted stem cells after brain damage. Front Cell Neurosci 2014;8:219
22. Xie K, Liu Y, Hao W, et al. Tenascin-C deficiency ameliorates Alzheimer's disease-related pathology in mice. Neurobiol Aging 2013;34: 2389-98
23. Bennett DA, Wilson RS, Schneider JA, et al. Natural history of mild cognitive impairment in older persons. Neurology 2002;59:198-205
24. McKhann G, Drachman D, Folstein M, et al. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 1984;34:939-44
25. Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of Patients for the clinician. J Psychiatr Res 1975;12:189-98
26. Consensus report of the Working Group on: "Molecular and Biochemical Markers of Alzheimer's Disease". The Ronald and Nancy Reagan Research Institute of the Alzheimer's Association and the National Institute on Aging Working Group. Neurobiol Aging 1998;19:109-16.
27. Mirra SS, Heyman A, McKeel D, et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991;41:479-86
28. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991;82:239-59
29. Hyman BT, Phelps CH, Beach TG, et al. National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease. Alzheimers Dement 2012;8:1-13
30. Ikonomovic MD, Abrahamson EE, Isanski BA, et al. Superior frontal cortex cholinergic axon density in mild cognitive impairment and early Alzheimer disease. Arch Neurol 2007;64:1312-7
31. Mufson EJ, Chen EY, Cochran EJ, et al. Entorhinal cortex beta-amyloid load in individuals with mild cognitive impairment. Exp Neurol 1999; 158:469-90
32. Schenk S, Muser J, Vollmer G, et al. Tenascin-C in serum: a questionable tumor marker. Int J Cancer 1995;61:443-9
33. Ikonomovic MD, Abrahamson EE, Isanski BA, et al. X-34 labeling of abnormal protein aggregates during the progression of Alzheimer's disease. Methods Enzymol 2006;412:123-44
34. Arnold SE, Hyman BT, Flory J, et al. The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. Cereb Cortex 1991; 1:103-16
35. Pike KE, Savage G, Villemagne VL, et al. Beta-amyloid imaging and memory in non-demented individuals: evidence for preclinical Alzheimer's disease. Brain 2007;130:2837-44
36. Price JL, McKeel DW, Jr., Buckles VD, et al. Neuropathology of nondemented aging: presumptive evidence for preclinical Alzheimer disease. Neurobiol Aging 2009;30:1026-36
37. Zagzag D, Friedlander DR, Miller DC, et al. Tenascin expression in astrocytomas correlates with angiogenesis. Cancer Res 1995;55:907-14
38. Koukoulis GK, Gould VE, Bhattacharyya A, et al. Tenascin in normal, reactive, hyperplastic, and neoplastic tissues: biologic and pathologic implications. Hum Pathol 1991;22:636-43
39. Eikelenboom P, Veerhuis R, Familian A, et al. Neuroinflammation in plaque and vascular beta-amyloid disorders: clinical and therapeutic implications. Neurodegener Dis 2008;5:190-3
40. Rozemuller AJ, van Gool WA, Eikelenboom P. The neuroinflammatory response in plaques and amyloid angiopathy in Alzheimer's disease: therapeutic implications. Curr Drug Targets CNS Neurol Disord 2005;4: 223-33
41. Zhang WW, Lempessi H, Olsson Y. Amyloid angiopathy of the human brain: immunohistochemical studies using markers for components of extracellular matrix, smooth muscle actin and endothelial cells. Acta Neuropathol 1998;96:558-63
42. Leins A, Riva P, Lindstedt R, et al. Expression of tenascin-C in various human brain tumors and its relevance for survival in patients with astrocytoma. Cancer 2003;98:2430-9
43. Natali PG, Nicotra MR, Bigotti A, et al. Comparative analysis of the expression of the extracellular matrix protein tenascin in normal human fetal, adult and tumor tissues. Int J Cancer 1991;47:811-6
44. Van Eldik LJ, Griffin WS. S100 beta expression in Alzheimer's disease: relation to neuropathology in brain regions. Biochim Biophys Acta 1994; 1223:398-403
45. Sheng JG, Mrak RE, Bales KR, et al. Overexpression of the neuritotrophic cytokine S100beta precedes the appearance of neuritic beta-amyloid plaques in APPV717F mice. J Neurochem 2000;74:295-301
46. Mrak RE, Sheng JG, Griffin WS. Correlation of astrocytic S100 beta expression with dystrophic neurites in amyloid plaques of Alzheimer's disease. J Neuropathol Exp Neurol 1996;55:273-9
47. Sheng JG, Mrak RE, Griffin WS. Neuritic plaque evolution in Alzheimer's disease is accompanied by transition of activated microglia from primed to enlarged to phagocytic forms. Acta Neuropathol 1997;94:1-5
48. Akiyama H, Barger S, Barnum S, et al. Inflammation and Alzheimer's disease. Neurobiol Aging 2000;21:383-421
49. Wyss-Coray T, Rogers J. Inflammation in Alzheimer disease-a brief review of the basic science and clinical literature. Cold Spring Harb Perspect Med 2012;2:a006346
50. Giulian D, Woodward J, Young DG, et al. Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization. J Neurosci 1988;8:2485-90
51. Brellier F, Tucker RP, Chiquet-Ehrismann R. Tenascins and their implications in diseases and tissue mechanics. Scand J Med Sci Sports 2009; 19:511-9
52. Pearson CA, Pearson D, Shibahara S, et al. Tenascin: cDNA cloning and induction by TGF-beta. Embo J 1988;7:2977-82
53. Chiovaro F, Chiquet-Ehrismann R, Chiquet M. Transcriptional regulation of tenascin genes. Cell Adh Migr 2015;9:34-47
54. Midwood K, Sacre S, Piccinini AM, et al. Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease. Nat Med 2009;15:774-80
55. Nakahara H, Gabazza EC, Fujimoto H, et al. Deficiency of tenascin C attenuates allergen-induced bronchial asthma in the mouse. Eur J Immunol 2006;36:3334-45
56. Mackie EJ, Halfter W, Liverani D. Induction of tenascin in healing wounds. J Cell Biol 1988;107:2757-67
57. Page TH, Charles PJ, Piccinini AM, et al. Raised circulating tenascin-C in rheumatoid arthritis. Arthritis Res Ther 2012;14:R260
58. Martin D, Brown-Luedi M, Chiquet-Ehrismann R. Tenascin-C signaling through induction of 14-3-3 tau. J Cell Biol 2003;160:171-5
59. Di Francesco L, Correani V, Fabrizi C, et al. 14-3-3epsilon marks the amyloid-stimulated microglia long-term activation. Proteomics 2012;12: 124-34
60. Layfield R, Fergusson J, Aitken A, et al. Neurofibrillary tangles of Alzheimer's disease brains contain 14-3-3 proteins. Neurosci Lett 1996;209: 57-60
61. Hashiguchi M, Sobue K, Paudel HK. 14-3-3zeta is an effector of tau protein phosphorylation. J Biol Chem 2000;275:25247-54
62. Agarwal-Mawal A, Qureshi HY, Cafferty PW, et al. 14-3-3 connects glycogen synthase kinase-3 beta to tau within a brain microtubuleassociated tau phosphorylation complex. J Biol Chem 2003;278:12722-8
63. Yuan Z, Agarwal-Mawal A, Paudel HK. 14-3-3 binds to and mediates phosphorylation of microtubule-associated tau protein by Ser9-phosphorylated glycogen synthase kinase 3beta in the brain. J Biol Chem 2004;279:26105-14
64. Khachaturian ZS. Diagnosis of Alzheimer's disease. Arch Neurol 1985; 42:1097-105
65. Klunk WE, Engler H, Nordberg A, et al. Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann Neurol 2004;55: 306-19
66. Curtis C, Gamez JE, Singh U, et al. Phase 3 trial of flutemetamol labeled with radioactive fluorine 18 imaging and neuritic plaque density. JAMA Neurol 2015;72:287-94
67. Clark CM, Pontecorvo MJ, Beach TG, et al. Cerebral PET with florbetapir compared with neuropathology at autopsy for detection of neuritic amyloid-beta plaques: a prospective cohort study. Lancet Neurol 2012; 11:669-78
68. Sabri O, Sabbagh MN, Seibyl J, et al. Florbetaben PET imaging to detect amyloid beta plaques in Alzheimer's disease: Phase 3 study. Alzheimers Dement 2015;11:964-74
69. Ikonomovic MD, Klunk WE, Abrahamson EE, et al. Post-mortem correlates of in vivo PiB-PET amyloid imaging in a typical case of Alzheimer's disease. Brain 2008;131:1630-45
70. Lockhart A, Lamb JR, Osredkar T, et al. PIB is a non-specific imaging marker of amyloid-beta (Abeta) peptide-related cerebral amyloidosis. Brain 2007;130:2607-15
71. Bacskai BJ, Frosch MP, Freeman SH, et al. Molecular imaging with Pittsburgh Compound B confirmed at autopsy: a case report. Arch Neurol 2007;64:431-4
72. Soares HD, Potter WZ, Pickering E, et al. Plasma biomarkers associated with the apolipoprotein E genotype and Alzheimer disease. Arch Neurol 2012;69:1310-7